Cite this paper:
Ruoyu LIU, Jun LIU, Haibin ZHANG. Positive selection analysis reveals the deep-sea adaptation of a hadal sea cucumber (Paelopatides sp.) to the Mariana Trench[J]. Journal of Oceanology and Limnology, 2021, 39(1): 266-281

Positive selection analysis reveals the deep-sea adaptation of a hadal sea cucumber (Paelopatides sp.) to the Mariana Trench

Ruoyu LIU1,2, Jun LIU1, Haibin ZHANG1
1 Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China
The Mariana Trench, the deepest trench on the earth, is ideal for deep-sea adaptation research due to its unique characters, such as the highest hydrostatic pressure on the Earth, constant ice-cold temperature, and eternal darkness. In this study, tissues of a the hadal holothurian (Paelopatides sp.) were fixed with RNA later in situ at ~6 501-m depth in the Mariana Trench, which, to our knowledge, is the deepest in-situ fixed animal sample. A high-quality transcript was obtained by de-novo transcriptome assembly. A maximum likelihood tree was constructed based on the single copy orthologs across nine species with their available omics data. To investigate deep-sea adaptation, 113 positively selected genes (PSGs) were identified in Paelopatides sp. Some PSGs such as microphthalmia-associated transcription factor (MITF) may contribute to the distinct phenotype of Paelopatides sp., including its translucent white body and degenerated ossicles. At least eight PSGs (transcription factor 7-like 2[TCF7L2], ETS-related transcription factor Elf-2-like [ELF2], PERQ amino acid-rich with GYF domain-containing protein[GIGYF], cytochrome c oxidase subunit 7a,[COX7A], type I thyroxine 5'-deiodinase[DIO1], translation factor GUF1[GUF1], SWI/SNF related-matrix-associated actin-dependent regulator of chromatin subfamily C and subfamily E, member 1[SMARCC] and[SMARCE1]) might be related to cold adaptation. In addition, at least nine PSGs (cell cycle checkpoint control protein[RAD9A], replication factor A3[RPA3], DNA-directed RNA polymerases I/Ⅱ/Ⅲ subunit RPABC1[POLR2E], putative TAR DNA-binding protein 43 isoform X2[TARDBP], ribonucleoside-diphosphate reductase subunit M1[RRM1], putative serine/threonine-protein kinase [SMG1], transcriptional regulator[ATRX], alkylated DNA repair protein alkB homolog 6[ALKBH6], and PLAC8 motif-containing protein[PLAC8]) may facilitate the repair of DNA damage induced by the high hydrostatic pressure, coldness, and high concentration of cadmium in the upper Mariana Trench.
Key words:    sea cucumber|Mariana Trench|deep-sea adaptation|positive selection analysis|translucent white body|ossicle degeneration   
Received: 2020-06-23   Revised: 2020-07-27
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Abbà S, Vallino M, Daghino S, Di Vietro L, Borriello R, Perotto S. 2011. A PLAC8-containing protein from an endomycorrhizal fungus confers cadmium resistance to yeast cells by interacting with Mlh3p. Nucleic Acids Research, 39(17):7 548-7 563,
Altschul S F, Madden T L, Schäffer A A, Zhang J H, Zhang Z, Miller W, Lipman D J. 1997. Gapped BLAST and PSIBLAST:a new generation of protein database search programs. Nucleic Acids Research, 25(17):3 389-3 402,
Anderson G B, Foote R H. 1975. Effects of low temperature upon subsequent nucleic acid and protein synthesis of rabbit embryos. Experimental Cell Research, 90(1):73-78,
Anderson T R, Rice T. 2006. Deserts on the sea floor:Edward Forbes and his azoic hypothesis for a lifeless deep ocean.Endeavour, 30(4):131-137,
Andrews S. 2010. FastQC:a quality control tool for high throughput sequence data. Babraham Bioinformatics,
Balny C, Mozhaev V V, Lange R. 1997. Hydrostatic pressure and proteins:basic concepts and new data. Comparative Biochemistry and Physiology Part A:Physiology, 116(4):299-304,
Bauerschmitt H, Funes S, Herrmann J M. 2008. The membranebound GTPase Guf1 promotes mitochondrial protein synthesis under suboptimal conditions. Journal of Biological Chemistry, 283(25):17 139-17 146,
Beliaev G M, Brueggeman P L. 1989. Deep Sea Ocean Trenches and Their Fauna. UC San Diego Scripps Institution of Oceanography Technical Report (Translated from Russian. The original book was published in Russian by Nauka Publishing House, Moscow, 1989), 255p.ISBN5-02-00,
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate:a practical and powerful approach to multiple testing.Journal of the Royal Statistical Society:Series B (Methodological), 57(1):289-300,
Bhagavan N V, Ha C E. 2015. DNA replication, repair, and mutagenesis. In:Bhagavan N V, Ha C E eds. Essentials of Medical Biochemistry. 2nd edn. Academic Press, Amsterdam. p.401-417,
Bianco A C, Kim B W. 2006. Deiodinases:implications of the local control of thyroid hormone action. Journal of Clinical Investigation, 116(10):2 571-2 579,
Buchfink B, Xie C, Huson D H. 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12(1):59-60,
Cannon J T, Kocot K M, Waits D S, Weese DA, Swalla BJ, Santos S R, Halanych K M. 2014. Phylogenomic resolution of the hemichordate and echinoderm clade.Current Biology, 24(23):2 827-2 832,
Carney R S. 2005. Zonation of deep biota on continental margins. In:Gibson R N, Atkinson R J A, Gordon J D M eds. Oceanography and Marine Biology-An Annual Review. Taylor & Francis. New York.
Chen S F, Zhou Y Q, Chen Y R, Gu J. 2018. FASTP:an ultrafast all-in-one FASTQ preprocessor. Bioinformatics, 34(17):i884-i890,
Cheng J, Hui M, Sha Z L. 2019. Transcriptomic analysis reveals insights into deep-sea adaptations of the dominant species, Shinkaia crosnieri (Crustacea:Decapoda:Anomura), inhabiting both hydrothermal vents and cold seeps. BMC Genomics, 20(1):388,
Chieu H D, Suwansa-ard S, Abramov T, Elizur A, Cummins S F. 2018. In vitro oocyte maturation by radial nerve extract and early development of the black sea cucumber(Holothuria leucospilota). Aquaculture, 495:247-254,
Danovaro R, Dell'Anno A, Pusceddu A. 2004. Biodiversity response to climate change in a warm deep sea. Ecology Letters, 7(9):821-828,
Darriba D, Taboada G L, Doallo R, Posada D. 2011. ProtTest 3:fast selection of best-fit models of protein evolution.Bioinformatics, 27(8):1 164-1 165,
De La Fuente R, Baumann C, Viveiros M M. 2011. Role of ATRX in chromatin structure and function:implications for chromosome instability and human disease.Reproduction, 142(2):221-234,
Dehcheshmeh I S, Karimi M M, Jafarisani M. 2018. Increased expression of CCAT2 LncRNA in non-melanoma skin cancer. International Journal of Health Studies, 4(1):1-4,
Dixon D R, Pruski A M, Dixon L R J. 2004. The effects of hydrostatic pressure change on DNA integrity in the hydrothermal-vent mussel Bathymodiolus azoricus:implications for future deep-sea mutagenicity studies.Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 552(1-2):235-246,
Downey R V, Fuchs M, Janussen D. 2018. Unusually diverse, abundant and endemic deep-sea sponge fauna revealed in the Sea of Okhotsk (NW Pacific Ocean). Deep Sea Research Part Ⅱ:Topical Studies in Oceanography, 154:47-58,
Fedeles B I, Singh V, Delaney J C, Li D Y, Essigmann J M. 2015. TheAlkB Family of Fe(Ⅱ)/α-Ketoglutarate-dependent Dioxygenases:repairing nucleic acid alkylation damage and beyond. Journal of Biological Chemistry, 290(34):20 734-20 742,
Feller G, Gerday C. 2003. Psychrophilic enzymes:hot topics in cold adaptation. Nature Reviews Microbiology, 1(3):200-208,
Finn R D, Clements J, Eddy S R. 2011. HMMER web server:interactive sequence similarity searching. Nucleic Acids Research, 39(Web Server issue):W29-W37,
Fisher F M, Kleiner S, Douris N, Fox E C, Mepani R J, Verdeguer F, Wu J, Kharitonenkov A, Flier J S, MaratosFlier E, Spiegelman B M. 2012. FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis. Genes & Development, 26(3):271-281,
Foote A D, Liu Y, Thomas G W C, Vinař T, Alföldi J, Deng J X, Dugan S, van Elk C E, Hunter M E, Joshi V, Khan Z, Kovar C, Lee S L, Lindblad-Toh K, Mancia A, Nielsen R, Qin X, Qu J X, Raney B J, Vijay N, Wolf J B W, Hahn M W, Muzny D M, Worley K C, Gilbert M T P, Gibbs R A. 2015. Convergent evolution of the genomes of marine mammals. Nature Genetics, 47(3):272-275,
Fry E A, Mallakin A, Inoue K. 2018. Translocations involving ETS family proteins in human cancer. Integrative Cancer Science and Therapeutics, 5(4):1-12,
Gereben B, Zavacki A M, Ribich S, Kim B W, Huang S A, Simonides W S, Zeold A, Bianco A C. 2008. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocrine Reviews, 29(7):898-938,
Gualerzi C O, Giuliodori A M, Pon C L. 2003. Transcriptional and post-transcriptional control of cold-shock genes.Journal of Molecular Biology, 331(3):527-539,
Haas B J, Papanicolaou A, Yassour M, Grabherr M, Blood P D, Bowden J, Couger M B, Eccles D, Li B, Lieber M, MacManes M D, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey C N, Henschel R, LeDuc R D, Friedman N, Regev A. 2013. De novo transcript sequence reconstruction from RNA-Seq using the Trinity platform for reference generation and analysis.Nature Protocols, 8(8):1 494-1 512,
Han B, Cai J Q, Gao W D, Meng X Q, Gao F, Wu P F, Duan C B, Wang R J, Dinislam M, Lin L, Kang C S, Jiang C L. 2018. Loss of ATRX suppresses ATM dependent DNA damage repair by modulating H3K9me3 to enhance temozolomide sensitivity in glioma. Cancer Letters, 419:280-290,
Hauswirth R, Haase B, Blatter M, Brooks S A, Burger D, Drogemuller C, Gerber V, Henke D, Janda J, Jude R, Magdesian K G, Matthews J M, Poncet P A, Svansson V, Tozaki T, Wilkinson-White L, Penedo M C T, Rieder S, Leeb T. 2012. Mutations in MITF and PAX3 cause "splashed white" and other white spotting phenotypes in horses. PLoS Genetics, 8(4):e1002653,
Hayman A R, Jones S J, Boyde A, Foster D, Colledge W H, Carlton M B, Evans M J, Cox T M. 1996. Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis.Development, 122(10):3 151-3 162.
Heyland A, Moroz L L. 2005. Cross-kingdom hormonal signaling:an insight from thyroid hormone functions in marine larvae. Journal of Experimental Biology, 208:4 355-4 361,
Hui M, Song C W, Liu Y, Li C L, Cui Z X. 2017. Exploring the molecular basis of adaptive evolution in hydrothermal vent crab Austinograea alayseae by transcriptome analysis. PLoS One, 12(5):e0178417,
Jamieson A. 2015. The Hadal Zone:Life in the Deepest Oceans. Cambridge University Press, Cambridge.
Jamieson A J, Gebruk A, Fujii T, Solan M. 2011. Functional effects of the hadal sea cucumber Elpidia atakama(Echinodermata:Holothuroidea, Elasipodida) reflect small-scale patterns of resource availability. Marine Biology, 158(12):2 695-2 703,
Janies D A, Witter Z, Linchangco G V, Foltz D W, Miller A K, Kerr A M, Jay J, Reid R W, Wray G A. 2016. EchinoDB, an application for comparative transcriptomics of deeplysampled clades of echinoderms. BMC Bioinformatics, 17:48,
Jin D X. 2018. Molecular Determinants of Mammary Differentiation and Breast Cancer Progression. PhD diss., Massachusetts Institute of Technology, Cambridge, Massachusetts, United States.
Jones P, Binns D, Chang H Y, Fraser M, Li W Z, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn A F, Sangrador-Vegas, Scheremetjew M, Yong S Y, Lopez R, Hunter S. 2014. InterProScan 5:genome-scale protein function classification. Bioinformatics, 30(9):1 236-1 240,
Kang S, Kim S, Park H. 2015. Transcriptome of the antarctic amphipod Gondogeneia antarctica and its response to pollutant exposure. Marine Genomics, 24:253-254,
Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Molecular Biology and Evolution, 30(4):772-780,
Kuzuhara T, Horikoshi M. 2004. A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing.Nature Structural & Molecular Biology, 11(3):275-283,
Ladner R D. 2001. The role of dUTPase and uracil-DNA repair in cancer chemotherapy. Current Protein & Peptide Science, 2(4):361-370,
Lan Y, Sun J, Tian R M, Bartlett D H, Li R S, Wong Y H, Zhang W P, Qiu J W, Xu T, He L S, Tabata H G, Qian P Y. 2017. Molecular adaptation in the world's deepest-living animal:insights from transcriptome sequencing of the hadal amphipod Hirondellea gigas. Molecular Ecology, 26(14):3 732-3 743,
Lan Y, Sun J, Xu T, Chen C, Tian R M, Qiu J W, Qian P Y. 2018. De novo transcriptome assembly and positive selection analysis of an individual deep-sea fish. BMC Genomics, 19:394,
Lan Y, Sun J, Zhang W P, Xu T, Zhang Y, Chen C, Feng D, Wang H B, Tao J, Qiu J W, Qian P Y. 2019. Host-symbiont interactions in deep-sea chemosymbiotic vesicomyid clams:insights from transcriptome sequencing. Frontiers in Marine Science, 6:680,
Leal L N, Romao J M, Hooiveld G J, Soberon F, Berends H, Boekshoten M V, Van Amburgh M E, Martín-Tereso J, Steele M A. 2018. Nutrient supply alters transcriptome regulation in adipose tissue of pre-weaning Holstein calves. PLoS One, 13(8):e0201929,
Lee Hufford G. 1968. Some Aspects of the Biology of the Deep Sea Holothuroid Paelopatides sp.. Oregon State University, Corvallis.
Li B, Dewey C N. 2011. RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12:323,
Li B, Ruotti V, Stewart R M, Thomson J A, Dewey C N. 2010.RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics, 26(4):493-500,
Li L, Stoeckert C J Jr, Roos D S. 2003. OrthoMCL:identification of ortholog groups for eukaryotic genomes.Genome Research, 13(9):2 178-2 189,
Li W Z, Godzik A. 2006. Cd-hit:a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics, 22(13):1 658-1 659,
Liang L Y, Chen J W, Li Y N, Zhang H B. 2020. Insights into high-pressure acclimation:comparative transcriptome analysis of sea cucumber Apostichopus japonicus at different hydrostatic pressure exposures. BMC Genomics, 21:68,
Liao Y L. 1997. Fauna Sinica:Phylum Echinodermata, Class Holothuroidea. Science Press, Beijing. (in Chinese)
Lieberman H B, Panigrahi S K, Hopkins K M, Wang L, Broustas C G. 2017. p53 and RAD9, the DNA damage response, and regulation of transcription networks.Radiation Research, 187(4):424-432,
Lim J, Thomas T, Cavicchioli R. 2000. Low temperature regulated DEAD-box RNA helicase from the antarctic archaeon, Methanococcoides burtonii. Journal of Molecular Biology, 297(3):553-567,
Lin A J, Zhang X H, Chen M M, Cao Q. 2007. Oxidative stress and DNA damages induced by cadmium accumulation.Journal of Environmental Sciences, 19(5):596-602,
Liu B H, Yip R K H, Zhou Z J. 2012. Chromatin remodeling, DNA damage repair and aging. Current Genomics, 13(7):533-547,
Liu R Y, Wang K, Liu J, Xu W J, Zhou Y, Zhu C L, Wu B S, Li Y X, Wang W, He S P, Feng C G, Zhang H B. 2020. De novo genome assembly of limpet Bathyacmaea lactea(Gastropoda:Pectinodontidae):the first reference genome of a deep-sea gastropod endemic to cold seeps. Genome Biology and Evolution, 12(6):905-910,
Lloyd J P B, Lang D, Zimmer A D, Causier B, Reski R, Davies B. 2018. The loss of SMG1 causes defects in quality control pathways in Physcomitrella patens. Nucleic Acids Research, 46(11):5 822-5 836,
Long K A, Nossa C W, Sewell M A, Putnam N H, Ryan J F. 2016. Low coverage sequencing of three echinoderm genomes:the brittle star Ophionereis fasciata, the sea star Patiriella regularis, and the sea cucumber Australostichopus mollis. Gigascience, 5(1):20,
Lu S Y, Li M T, Lin Y L. 2010. Mitf induction by RANKL is critical for osteoclastogenesis. Molecular Biology of the Cell, 21(10):1 763-1 771,
Lu S Y, Li M T, Lin Y L. 2014. Mitf regulates osteoclastogenesis by modulating NFATc1 activity. Experimental Cell Research, 328(1):32-43,
Martinez M I, Solís-Marín F A, Penchaszadeh P E. 2019. First report of Paelopatides (Synallactida, Synallactidae) for the SW Atlantic, with description of a new species from the deep-sea off Argentina. Zoologischer Anzeiger, 278:21-27,
Maurer S F, Fromme T, Grossman L I, Hüttemann M, Klingenspor M. 2015. The brown and brite adipocyte marker Cox7a1 is not required for non-shivering thermogenesis in mice. Scientific Reports, 5:17 704,
McGaugh S E, Gross J B, Aken B, Blin M, Borowsky R, Chalopin D, Hinaux H, Jeffery W R, Keene A, Ma L, Minx P, Murphy D, O'Quin K E, Rétaux S, Rohner N, Searle S W J, Stahl B A, Tabin C, Volff J N, Yoshizawa M, Warren W C. 2014. The cavefish genome reveals candidate genes for eye loss. Nature Communications, 5:5307,
Mehr S, Verdes A, Desalle R, Sparks J, Pieribone V, Gruber D F. 2015. Transcriptome sequencing and annotation of the polychaete Hermodice carunculata (Annelida, Amphinomidae). BMC Genomics, 16:445,
Miller A K, Kerr A M, Paulay G, Reich M, Wilson N G, Carvajal J I, Rouse G W. 2017. Molecular phylogeny of extant Holothuroidea (Echinodermata). Molecular Phylogenetics and Evolution, 111:110-131,
Mitra J, Guerrero E N, Hegde P M, Liachko N F, Wang H B, Vasquez V, Gao J L, Pandey A, Taylor J P, Kraemer B C, Wu P, Boldogh I, Garruto R M, Mitra S, Rao K S, Hegde M L. 2019. Motor neuron disease-associated loss of nuclear TDP-43 is linked to DNA double-strand break repair defects. Proceedings of the National Academy of Sciences of the United States of America, 116(10):4 696-4 705,
Moore K J. 1995. Insight into the microphthalmia gene. Trends in Genetics, 11(11):442-448,
Mozhaev V V, Heremans K, Frank J, Masson P, Balny C. 1996.High pressure effects on protein structure and function.Proteins, 24(1):81-91,<81::AID-PROT6>3.0.CO;2-R.
Musilova Z, Cortesi F, Matschiner M, Davies W I L, Patel J S, Stieb S M, de Busserolles F, Malmstrøm M, Tørresen O K, Brown C J, Mountford J K, Hanel R, Stenkamp D L, Jakobsen K S, Carleton K L, Jentoft S, Marshall J, Salzburger W. 2019. Vision using multiple distinct rod opsins in deep-sea fishes. Science, 364(6440):588-592,
Nguyen N T, Fisher D E. 2019. MITF and UV responses in skin:from pigmentation to addiction. Pigment Cell & Melanoma Research, 32(2):224-236,
Nie M M, Tan X G, Lu Y L, Wu Z H, Li J, Xu D D, Zhang P J, You F. 2019. Network of microRNA-transcriptional factor-mRNA in cold response of turbot Scophthalmus maximus. Fish Physiology and Biochemistry, 45(2):583-597,
Panicker V, Cluett C, Shields B, Murray A, Parnell K S, Perry J R B, Weedon M N, Singleton A, Hernandez D, Evans J, Durant C, Ferrucci L, Melzer D, Saravanan P, Visser T J, Ceresini G, Hattersley A T, Vaidya B, Dayan C M, Frayling T M. 2008. A common variation in deiodinase 1 gene DIO1 is associated with the relative levels of free thyroxine and triiodothyronine. The Journal of Clinical Endocrinology & Metabolism, 93(8):3 075-3 081,
Pease D C. 1946. Hydrostatic pressure effects upon the spindle figure and chromosome movement. Ⅱ. Experiments on the meiotic divisions of tradescantia pollen mother cells.The Biological Bulletin, 91(2):145-169,
Peter D, Weber R, Sandmeir F, Wohlbold L, Helms S, Bawankar P, Valkov E, Igreja C, Izaurralde E. 2017.GIGYF1/2 proteins use auxiliary sequences to selectively bind to 4EHP and repress target mRNA expression. Genes & Development, 31(11):1 147-1 161,
Phadtare S, Alsina J, Inouye M. 1999. Cold-shock response and cold-shock proteins. Current Opinion in Microbiology, 2(2):175-180,
Purcell S W, Samyn Y, Conand C. 2012. Commercially Important Sea Cucumbers of the World. FAO, Roma.
Reich A, Dunn C, Akasaka K, Wessel G. 2015. Phylogenomic analyses of echinodermata support the sister groups of asterozoa and echinozoa. PLoS One, 10(3):e0119627,
Sanderson M J. 2003. r8s:inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics, 19(2):301-302,
Schmutz S M, Berryere T G, Dreger D L. 2009. MITF and white spotting in dogs:a population study. Journal of Heredity, 100(S1):S66-S74,
Simonato F, Campanaro S, Lauro F M, Vezzi A, D'Angelo M, Vitulo N, Valle G, Bartlett D H. 2006. Piezophilic adaptation:a genomic point of view. Journal of Biotechnology, 126(1):11-25,
Smirnov A V, Gebruk A V, Galkin S V, Shank T. 2000. New species of holothurian (Echinodermata:Holothuroidea)from hydrothermal vent habitats. Journal of the Marine Biological Association of the United Kingdom, 80(2):321-328,
Somero G N. 2003. Protein adaptations to temperature and pressure:complementary roles of adaptive changes in amino acid sequence and internal milieu. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 136(4):577-591,
Stadtman E R, Van Remmen H, Richardson A, Wehr N B, Levine R L. 2005. Methionine oxidation and aging.Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1703(2):135-140,
Stamatakis A. 2014. RAxML version 8:a tool for phylogenetic analysis and post-analysis of large phylogenies.Bioinformatics, 30(9):1 312-1 313,
Sun J, Chen C, Miyamoto N, Li R S, Sigwart J D, Xu T, Sun Y N, Wong W C, Ip J C H, Zhang W P, Lan Y, Bissessur D, Watsuji T O, Watanabe H K, Takaki Y, Ikeo K, Fujii N, Yoshitake K, Qiu J W, Takai K, Qian P Y. 2020. The Scaly-foot Snail genome and implications for the origins of biomineralised armour. Nature Communications, 11(1):1657,
Sun J, Zhang Y, Xu T, Zhang Y, Mu H W, Zhang Y J, Lan Y, Fields C J, Hui J H L, Zhang W P, Li R S, Nong W Y, Cheung F K M, Qiu J W, Qian P Y. 2017. Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes. Nature Ecology & Evolution, 1(5):0121,
Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56(4):564-577,
Tang C, Wang Y W, Lan D L, Feng X H, Zhu X, Nie P T, Yue H. 2015. Analysis of gene expression profiles reveals the regulatory network of cold-inducible RNA-binding protein mediating the growth of BHK-21 cells. Cell Biology International, 39(6):678-689,
The R Core Team. 2016. R:A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Thieringer H A, Jones P G, Inouye M. 1998. Cold shock and adaptation. Bioessays, 20(1):49-57,<49::AID-BIES8>3.0.CO;2-N.
Wang K, Shen Y J, Yang Y Z, Gan X N, Liu G C, Hu K, Li Y X, Gao Z M, Zhu L, Yan G Y, He L S, Shan X J, Yang L D, Lu S X, Zeng H H, Pan X Y, Liu C, Yuan Y, Feng C G, Xu W J, Zhu C L, Xiao W H, Dong Y, Wang W, Qiu Q, He S P. 2019. Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation.Nature Ecology & Evolution, 3(5):823-833,
Waterhouse R M, Seppey M, Simao F A, Manni M, Ioannidis P, Klioutchnikov G, Kriventseva E V, Zdobnov E M. 2018. BUSCO applications from quality assessments to gene prediction and phylogenomics. Molecular Biology and Evolution, 35(3):543-548,
Welty C J, Sousa M L, Dunnivant F M, Yancey P H. 2018.High-density element concentrations in fish from subtidal to hadal zones of the Pacific Ocean. Heliyon, 4(10):e00840,
Wilton D J, Ghosh M, Chary K V A, Akasaka K, Williamson M P. 2008. Structural change in a B-DNA helix with hydrostatic pressure. Nucleic Acids Research, 36(12):4 032-4 037,
Xing L L, Sun L N, Liu S L, Wan Z X, Li X N, Miao T, Zhang L B, Bai Y C, Yang H S. 2018. Growth, histology, ultrastructure and expression of MITF and astacin in the pigmentation stages of green, white and purple morphs of the sea cucumber, Apostichopus japonicus. Aquaculture Research, 49(1):177-187,
Yang H S, Zhou Y, Zhang T, Yuan X T, Li X X, Liu Y, Zhang F S. 2006. Metabolic characteristics of sea cucumber Apostichopus japonicus (Selenka) during aestivation.Journal of Experimental Marine Biology and Ecology, 330(2):505-510,
Yang L D, Wang Y, Zhang Z L, He S P. 2015. Comprehensive transcriptome analysis reveals accelerated genic evolution in a Tibet Fish, Gymnodiptychus pachycheilus. Genome Biology and Evolution, 7(1):251-261,
Yang Z H, dos Reis M. 2011. Statistical properties of the branch-site test of positive selection. Molecular Biology and Evolution, 28(3):1 217-1 228,
Yang Z H. 2007. PAML 4:phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8):1 586-1 591,
Yano Y, Nakayama A, Ishihara K, Saito H. 1998. Adaptive changes in membrane lipids of barophilic bacteria in response to changes in growth pressure. Applied and Environmental Microbiology, 64(2):479-485,
Zhang J Z, Nielsen R, Yang Z H. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution, 22(12):2 472-2 479,
Zhang J, Sun Q L, Luan Z D, Lian C, Sun L. 2017a.Comparative transcriptome analysis of Rimicaris sp.reveals novel molecular features associated with survival in deep-sea hydrothermal vent. Scientific Reports, 7(1):2 000,
Zhang Y J, Sun J, Chen C, Watanabe H K, Feng D, Zhang Y, Chiu J M Y, Qian P Y, Qiu J W. 2017b. Adaptation and evolution of deep-sea scale worms (Annelida:Polynoidae):insights from transcriptome comparison with a shallow-water species. Scientific Reports, 7(1):46205,
Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9:40,
Zhang Z, Xiao J F, Wu J Y, Zhang H Y, Liu G M, Wang X M, Dai L. 2012. ParaAT:A parallel tool for constructing multiple protein-coding DNA alignments. Biochemical and Biophysical Research Communications, 419(4):779-781,
Zhao H, Wang J, Han Y Q, Huang Z, Ying J M, Bi X Y, Zhao J J, Fang Y, Zhou H T, Zhou J G, Li Z Y, Zhang Y F, Yang X, Yan T, Wang L F, Torbenson M S, Cai J Q. 2011.ARID2:a new tumor suppressor gene in hepatocellular carcinoma. Oncotarget, 2(11):886-891,
Zheng P, Wang M X, Li C L, Sun X Q, Wang X C, Sun Y, Sun S. 2017. Insights into deep-sea adaptations and hostsymbiont interactions:a comparative transcriptome study on Bathymodiolus mussels and their coastal relatives.Molecular Ecology, 26(19):5 133-5 148,
Zou Y, Liu Y Y, Wu X M, Shell S M. 2006. Functions of human replication protein A (RPA):from DNA replication to DNA damage and stress responses. Journal of Cellular Physiology, 208(2):267-273,
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